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Antibiotics
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Research of Antimicrobial Resistance in the Food Chain
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Research of Antimicrobial Resistance in the Food Chain

A special issue of Antibiotics (ISSN 2079-6382). This special issue belongs to the section "Mechanism and Evolution of Antibiotic Resistance".

Deadline for manuscript submissions: closed (29 February 2024) | Viewed by 23418

Special Issue Editors

Dr. Krzysztof Skowron

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Guest Editor
Department of Microbiology, Nicolaus Copernicus University in Toruń, L. Rydygier Collegium Medicum in Bydgoszcz, 85-094 Bydgoszcz, Poland
Interests: food microbiology; environmental microbiology; medical microbiology; assessment of prevalence and characterization of Listeria monocytogenes strains; evaluation of the effectiveness of physical, chemical and biological antimicrobial activities; antibiotic resistance and virulence factors of microorganisms; bacterial biofilms and methods of their eradication; techniques of excrements and animal byproducts hygienization; molecular microbiology
Special Issues, Collections and Topics in MDPI journals
Dr. Joanna Kwiecińska-Piróg

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Guest Editor
Department of Microbiology, Nicolaus Copernicus University in Toruń, L. Rydygier Collegium Medicum in Bydgoszcz, 85-094 Bydgoszcz, Poland
Interests: medical microbiology; assessment of prevalence and characterization of Proteus mirabilis strains; evaluation of the effectiveness of physical, chemical and biological antimicrobial activities; antibiotic resistance and virulence factors of microorganisms; bacterial biofilms and methods of their eradication
Special Issues, Collections and Topics in MDPI journals
Dr. Katarzyna Grudlewska-Buda

E-Mail Website
Guest Editor
Department of Microbiology, Nicolaus Copernicus University in Toruń, L. Rydygier Collegium Medicum in Bydgoszcz, 85-094 Bydgoszcz, Poland
Interests: food microbiology; environmental microbiology; medical microbiology; assessment of prevalence and characterization of Listeria monocytogenes and Escherichia coli strains; evaluation of the effectiveness of physical, chemical and biological antimicrobial activities; antibiotic resistance and virulence factors of microorganisms; bacterial biofilms and methods of their eradication; techniques of excrements and animal byproducts hygienization; molecular microbiology

Special Issue Information

Dear Colleagues,

Increasing the antimicrobial resistance of bacteria and fungi is major challenge that is faced worldwide. One of the most common reasons for this is the use of antimicrobials in animal breeding and food processing. In farms, antimicrobials are commonly used in the prophylaxis of infectious diseases in animals, in order to reduce the risk of infection transmission. This occurs as antimicrobials are used as forage to improve the growth of animals. If antimicrobials remain in animals’ tissues and organs, the consumption of eggs, milk, honey, can adversely affect consumer health. Antibiotics, even in small doses opver a longer period, can promote the appearance of a multidrug resistant strain.

Antimicrobial resistance in food chains is a very important topic. This Special Issue aims to present the newest information and results from studies related to the use of antimicrobials in food chains. Research areas may include (but are not limited to) the following:

  • The occurrence of antimicrobials in food products and in food-processing environments;
  • The health risk associated with antimicrobials in food products;
  • The effect of antibiotics present in food on the human gut microbiome;
  • The fate of antibiotics in food chains and the environment;
  • The acquiring of antimicrobial resistance;
  • Antimicrobial resistance genes (ARG) and their transfer.

Dr. Krzysztof Skowron
Dr. Joanna Kwiecińska-Piróg
Dr. Katarzyna Grudlewska-Buda
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Antibiotics is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2900 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • antibiotics
  • food chain
  • multi-drug resistance
  • antimicrobial resistance
  • emerging pathogens
  • antibiotics resistance genes
  • transmission
  • microbiome

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Published Papers (8 papers)

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Research

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14 pages, 2382 KiB  
Article
Rumi and Pasteurized Kareish Cheeses Are a Source of β-Lactam-Resistant Salmonella in the Nile Delta Region of Egypt: Insights into Their Incidence, AMR Pattern, Genotypic Determinants of Virulence and β-Lactam Resistance
by Fatma Elzhraa, Maha Al-Ashmawy, Mohammed El-Sherbini, Ahmed M. El-Sebaey, Csilla Mohácsi-Farkas, Gabriella Kiskó and Ágnes Belák
Antibiotics 2024, 13(5), 454; https://doi.org/10.3390/antibiotics13050454 - 16 May 2024
Cited by 1 | Viewed by 1205
Abstract
The spread of superbugs in dairy products can jeopardize global public health. To date, information on the incidence rates of virulent and β-lactams-resistant (BLR) Salmonella in cheeses from rural areas of Egypt has been lacking. Biochemical, serological, antibiotic susceptibility, and multiplex PCR (M-PCR) [...] Read more.
The spread of superbugs in dairy products can jeopardize global public health. To date, information on the incidence rates of virulent and β-lactams-resistant (BLR) Salmonella in cheeses from rural areas of Egypt has been lacking. Biochemical, serological, antibiotic susceptibility, and multiplex PCR (M-PCR) tests were performed to identify and characterize Salmonella isolates. In this study, 44 (15.71%) Salmonella isolates of eight different serotypes were recovered from 280 samples of Rumi and pasteurized Kariesh cheeses across the Nile Delta region of Egypt. The most predominant serotypes were S. Typhimurium, S. Enteritidis, and S. Infantis. The virulence genes (invA, stn, and hilA) were identified in all isolates. However, spvC was only detected in S. Typhimurium. The highest resistance was developed against Erythromycin and Clindamycin (90.91%), followed by Ceftazidime and Cephalothin (84.09%). Meropenem and colistin were the most effective antibiotics. A high proportion (79.55%) of multi-drug resistance (MDR) isolates carried narrow spectrum (NS), extended-spectrum (ES), and AmpC-BLR genes. The blaOXA-1, blaOXA-2, blaTEM-1, blaCTX-M, blaCMY-1, and blaCMY-2 BLR genes were positive in 37.04%, 29.63%, 25.93%, 14.81%, 37.04%, and 3.70% of isolates, respectively. In conclusion, a high prevalence of virulence and BLR genes harboring Salmonella strains in Egyptian cheeses is considered a great threat to public health. Full article
(This article belongs to the Special Issue Research of Antimicrobial Resistance in the Food Chain)
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17 pages, 1508 KiB  
Article
Assessment of Prevalence and Diversity of Antimicrobial Resistant Escherichia coli from Retail Meats in Southern California
by Katie Yen Lee, Kurtis Lavelle, Anny Huang, Edward Robert Atwill, Maurice Pitesky and Xunde Li
Antibiotics 2023, 12(4), 782; https://doi.org/10.3390/antibiotics12040782 - 19 Apr 2023
Cited by 9 | Viewed by 2954
Abstract
Retail meat products may serve as reservoirs and conduits for antimicrobial resistance, which is frequently monitored using Escherichia coli as indicator bacteria. In this study, E. coli isolation was conducted on 221 retail meat samples (56 chicken, 54 ground turkey, 55 ground beef, [...] Read more.
Retail meat products may serve as reservoirs and conduits for antimicrobial resistance, which is frequently monitored using Escherichia coli as indicator bacteria. In this study, E. coli isolation was conducted on 221 retail meat samples (56 chicken, 54 ground turkey, 55 ground beef, and 56 pork chops) collected over a one-year period from grocery stores in southern California. The overall prevalence of E. coli in retail meat samples was 47.51% (105/221), with E. coli contamination found to be significantly associated with meat type and season of sampling. From antimicrobial susceptibility testing, 51 isolates (48.57%) were susceptible to all antimicrobials tested, 54 (51.34%) were resistant to at least 1 drug, 39 (37.14%) to 2 or more drugs, and 21 (20.00%) to 3 or more drugs. Resistance to ampicillin, gentamicin, streptomycin, and tetracycline were significantly associated with meat type, with poultry counterparts (chicken or ground turkey) exhibiting higher odds for resistance to these drugs compared to non-poultry meats (beef and pork). From the 52 E. coli isolates selected to undergo whole-genome sequencing (WGS), 27 antimicrobial resistance genes (ARGs) were identified and predicted phenotypic AMR profiles with an overall sensitivity and specificity of 93.33% and 99.84%, respectively. Clustering assessment and co-occurrence networks revealed that the genomic AMR determinants of E. coli from retail meat were highly heterogeneous, with a sparsity of shared gene networks. Full article
(This article belongs to the Special Issue Research of Antimicrobial Resistance in the Food Chain)
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15 pages, 3002 KiB  
Article
Assessment of Heavy Metals Contamination and Antimicrobial Drugs Residue in Broiler Edible Tissues in Bangladesh
by Shaikh Mohammad Bokhtiar, Mohammad Rafiqul Islam, Md. Jisan Ahmed, Abdur Rahman and Kazi Rafiq
Antibiotics 2023, 12(4), 662; https://doi.org/10.3390/antibiotics12040662 - 28 Mar 2023
Cited by 5 | Viewed by 2733
Abstract
There are substantial public health consequences when hazardous heavy metal contaminants and antimicrobial drug residues are present in broiler edible tissues. This study aimed to assess the concentration of antimicrobial drugs and heavy metals residues in broiler meat, bones and edible composites (combinations [...] Read more.
There are substantial public health consequences when hazardous heavy metal contaminants and antimicrobial drug residues are present in broiler edible tissues. This study aimed to assess the concentration of antimicrobial drugs and heavy metals residues in broiler meat, bones and edible composites (combinations of liver, kidney and gizzard). Samples were collected from different types of broiler farms, broiler wet meat markets and supermarkets, covering all five divisions of Bangladesh. The antimicrobial drug and heavy metal residues were analyzed by uHPLC and ICP-MS, respectively. In addition, a cross-sectional survey was conducted among broiler meat consumers in the study areas to evaluate their attitude towards the consumption of broiler meat. The survey clearly stated that broiler meat consumers in Bangladesh have a negative attitude toward the consumption of broiler meat, although all respondents reported to eat broiler meat regularly. The antibiotic with the highest prevalence of residues in broiler edible tissues was oxytetracycline, followed by doxycycline, sulphadiazine and chloramphenicol. On the other hand, all collected broiler edible tissues contained chromium and lead, followed by arsenic. The fact of the matter is that the antimicrobial drugs and heavy metals residues were found to be below the maximum residue limit (MRL), except for the lead content. In addition, the broiler meat samples from supermarkets had lower levels of antimicrobial drugs and heavy metals residue compared to the broiler meat collected from various types of farms and broiler wet meat markets. Irrespective of the source, broiler meat was found to contain antimicrobial drugs and heavy metals residues below the MRL, except for lead, suggesting that broiler meat is safe for human consumption. Therefore, raising public awareness regarding misconceptions about broiler meat consumption among consumers would be warranted. Full article
(This article belongs to the Special Issue Research of Antimicrobial Resistance in the Food Chain)
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13 pages, 1055 KiB  
Article
Ciprofloxacin Concentrations 1/1000th the MIC Can Select for Antimicrobial Resistance in N. gonorrhoeae—Important Implications for Maximum Residue Limits in Food
by Natalia González, Saïd Abdellati, Irith De Baetselier, Jolein Gyonne Elise Laumen, Christophe Van Dijck, Tessa de Block, Sheeba Santhini Manoharan-Basil and Chris Kenyon
Antibiotics 2022, 11(10), 1430; https://doi.org/10.3390/antibiotics11101430 - 18 Oct 2022
Cited by 7 | Viewed by 2533
Abstract
Background: Concentrations of fluoroquinolones up to 200-fold lower than the minimal inhibitory concentration (MIC) have been shown to be able to select for antimicrobial resistance in E. coli and Salmonella spp. (the minimum selection concentration—MSC). We hypothesized that the low concentrations of quinolones [...] Read more.
Background: Concentrations of fluoroquinolones up to 200-fold lower than the minimal inhibitory concentration (MIC) have been shown to be able to select for antimicrobial resistance in E. coli and Salmonella spp. (the minimum selection concentration—MSC). We hypothesized that the low concentrations of quinolones found in meat may play a role in the genesis of quinolone resistance in Neisseria gonorrhoeae. We aimed to (i) establish the ciprofloxacin MSC for N. gonorrhoeae and (ii) assess if, at the ecological level, the prevalence of gonococcal ciprofloxacin resistance is associated with the concentration of quinolones used in food animal production, which is an important determinant of long-term low-dose exposure to ciprofloxacin in humans. Methods: (i) To assess if subinhibitory ciprofloxacin concentrations could select for de novo generated resistant mutants, a susceptible WHO-P N. gonorrhoeae isolate was serially passaged at 1, 1:10, 1:100 and 1:1000 of the ciprofloxacin MIC of WHO-P (0.004 mg/L) on GC agar plates. (ii) Spearman’s correlation was used to assess the association between the prevalence of ciprofloxacin resistance in N. gonorrhoeae and quinolone use for animals and quinolone consumption by humans. Results: Ciprofloxacin concentrations as low as 0.004 µg/L (1/1000 of the MIC of WHO-P) were able to select for ciprofloxacin resistance. The prevalence of ciprofloxacin resistance in N. gonorrhoeae was positively associated with quinolone use for food animals (ρ = 0.47; p = 0.004; N = 34). Conclusion: Further individual level research is required to assess if low doses of ciprofloxacin from ingested foodstuffs are able to select for ciprofloxacin resistance in bacteria colonizing humans and other species. Full article
(This article belongs to the Special Issue Research of Antimicrobial Resistance in the Food Chain)
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15 pages, 1596 KiB  
Article
Influence of Single Dose Enrofloxacin Injection on Development of Fluoroquinolone Resistance in Campylobacter jejuni in Calves
by Debora Brito Goulart, Ashenafi Feyisa Beyi, Zuowei Wu, Mehmet Cemal Adiguzel, Samantha Wilson, Changyun Xu, Jinji Pang, Renee Dewell, Grant A. Dewell, Paul J. Plummer, Qijing Zhang and Orhan Sahin
Antibiotics 2022, 11(10), 1407; https://doi.org/10.3390/antibiotics11101407 - 13 Oct 2022
Cited by 5 | Viewed by 2014
Abstract
Fluoroquinolone (FQ) resistance in a major foodborne bacterial pathogen, Campylobacter jejuni, derived from cattle has recently become prevalent and poses a significant public health concern. However, the underlying factors for this increase are not entirely clear. To evaluate the effect of enrofloxacin [...] Read more.
Fluoroquinolone (FQ) resistance in a major foodborne bacterial pathogen, Campylobacter jejuni, derived from cattle has recently become prevalent and poses a significant public health concern. However, the underlying factors for this increase are not entirely clear. To evaluate the effect of enrofloxacin treatment on FQ-resistance development in C. jejuni, 35 commercial calves were equally divided into five groups (Groups 1–5) and were orally inoculated with FQ-susceptible (FQ-S) C. jejuni. Eight days later, Groups 4 and 5 were challenged with Mannheimia haemolytica via a transtracheal route to induce a respiratory disease; after 8 days, Groups 2, 3, 4, and 5 were injected subcutaneously with enrofloxacin (7.5 mg/kg for Groups 2 and 4, and 12.5 mg/kg for Groups 3 and 5). Colonization levels by FQ-resistant (FQ-R) and FQ-S Campylobacter in rectal feces were determined via differential culture throughout the experiment. Before oral inoculation with C. jejuni, only five calves were naturally colonized by Campylobacter, four of which were also colonized by FQ-R C. jejuni (three in Group 1 and one in Group 3). Soon after the oral inoculation, almost all calves in the groups became stably colonized by FQ-S C. jejuni (~3–6 log10 CFU/g), except that the four calves that were pre-colonized before inoculation remained positive with both FQ-R and FQ-S C. jejuni. Following enrofloxacin administration, C. jejuni colonization declined sharply and rapidly in all treated groups to undetectable levels; however, the vast majority of the animals were recolonized by C. jejuni at comparable levels 72 h after the treatment. Notably, no FQ-R C. jejuni was detected in any of the calves that received enrofloxacin, regardless of the drug dose used or disease status of the animals. The lack of detection of FQ-R C. jejuni was likely due to the localized high concentration of the antibiotic in the intestine, which may have prevented the emergence of the FQ-R mutant. These findings indicate that single-dose enrofloxacin use in cattle poses a low risk for selection of de novo FQ-R mutants in C. jejuni. Full article
(This article belongs to the Special Issue Research of Antimicrobial Resistance in the Food Chain)
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13 pages, 2578 KiB  
Article
Occurrence and Molecular Characterization of Multidrug-Resistant Vegetable-Borne Listeria monocytogenes Isolates
by Zizipho Ntshanka, Temitope C. Ekundayo, Erika M. du Plessis, Lise Korsten and Anthony I. Okoh
Antibiotics 2022, 11(10), 1353; https://doi.org/10.3390/antibiotics11101353 - 4 Oct 2022
Cited by 4 | Viewed by 2470
Abstract
Fresh vegetables play a significant role in the human diet. However, ready-to-eat (RTE) vegetables have been associated with increasing foodborne outbreaks including L. monocytogenes, which is a common human pathogen associated with foodborne infections resulting in listeriosis. This study aims to assess [...] Read more.
Fresh vegetables play a significant role in the human diet. However, ready-to-eat (RTE) vegetables have been associated with increasing foodborne outbreaks including L. monocytogenes, which is a common human pathogen associated with foodborne infections resulting in listeriosis. This study aims to assess the resistance of vegetable-borne L. monocytogenes to antibiotics. L. monocytogenes was isolated and molecularly characterized using polymerase chain reaction (PCR) from 17 RTE vegetable samples. The confirmed L. monocytogenes was further assessed for phenotypic and genotypic antibiotic resistance using the disc diffusion test and PCR primers targeting six antibiotic classes and thirty-one related antibiotic resistance genes (ARGs), respectively. The results revealed that Listeria counts ranged from 1.60 to 3.44 log10 CFU/g in the samples. The isolates exhibited high resistance against penicillin G, erythromycin, vancomycin, tetracycline, trimethoprim-sulfamethoxazole, and nitrofurantoin among the 108 isolates tested. A total of 71 multiple antibiotic resistance (MAR) phenotypes were observed in the isolates, which ranged from resistance to 3 to 13 antibiotics. The MAR index was ˃0.2 in 97% of the isolates. Some of the highly detected ARG subtypes included SulI (100%), TEM (76.9%), tetA (59%), and tetM (54.7%). The findings show a high occurrence of multidrug-resistant L. monocytogenes and clinical ARGs in fresh vegetables, which constitutes an immediate danger for the health security of the public. Full article
(This article belongs to the Special Issue Research of Antimicrobial Resistance in the Food Chain)
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10 pages, 289 KiB  
Article
High Fecal Prevalence of mcr-Positive Escherichia coli in Veal Calves at Slaughter in France
by Maryse Michèle Um, Véronique Dupouy, Nathalie Arpaillange, Clémence Bièche-Terrier, Frédéric Auvray, Eric Oswald, Hubert Brugère and Delphine Bibbal
Antibiotics 2022, 11(8), 1071; https://doi.org/10.3390/antibiotics11081071 - 8 Aug 2022
Cited by 2 | Viewed by 1750
Abstract
The aim of this study was to determine the percentage of healthy veal calves carrying mcr-positive E. coli strains at the time of slaughter in France. Fecal samples were selectively screened for mcr-positive E. coli isolates using media supplemented with colistin. [...] Read more.
The aim of this study was to determine the percentage of healthy veal calves carrying mcr-positive E. coli strains at the time of slaughter in France. Fecal samples were selectively screened for mcr-positive E. coli isolates using media supplemented with colistin. Screening for mcr genes was also carried out in E. coli isolates resistant to critically important antimicrobials used in human medicine recovered from the same fecal samples. Overall, 28 (16.5%) out of the 170 veal calves tested carried mcr-positive E. coli. As some calves carried several non-redundant mcr-positive strains, 41 mcr-positive E. coli were recovered. Thirty-one and seven strains were positive for mcr-1 and mcr-3 genes, respectively, while no strain was positive for the mcr-2 gene. Co-carriage of mcr-1 and mcr-3 was identified in three strains. All mcr-positive E. coli isolates, except one, were multidrug-resistant, with 56.1% being ciprofloxacin-resistant and 31.7% harboring blaCTX-M genes. All mcr-3-positive E. coli carried blaCTX-M genes, mainly blaCTX-M-55. This study highlights the high prevalence of mcr-positive E. coli strains in feces of veal calves at the time of slaughter. It also points out the multidrug (including ciprofloxacin) resistance of such strains and the co-occurrence of mcr-3 genes with blaCTX-M-55 genes. Full article
(This article belongs to the Special Issue Research of Antimicrobial Resistance in the Food Chain)

Review

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29 pages, 1363 KiB  
Review
Antibiotic Resistance in Selected Emerging Bacterial Foodborne Pathogens—An Issue of Concern?
by Katarzyna Grudlewska-Buda, Justyna Bauza-Kaszewska, Natalia Wiktorczyk-Kapischke, Anna Budzyńska, Eugenia Gospodarek-Komkowska and Krzysztof Skowron
Antibiotics 2023, 12(5), 880; https://doi.org/10.3390/antibiotics12050880 - 9 May 2023
Cited by 16 | Viewed by 6660
Abstract
Antibiotic resistance (AR) and multidrug resistance (MDR) have been confirmed for all major foodborne pathogens: Campylobacter spp., Salmonella spp., Escherichia coli and Listeria monocytogenes. Of great concern to scientists and physicians are also reports of antibiotic-resistant emerging food pathogens—microorganisms that have not previously [...] Read more.
Antibiotic resistance (AR) and multidrug resistance (MDR) have been confirmed for all major foodborne pathogens: Campylobacter spp., Salmonella spp., Escherichia coli and Listeria monocytogenes. Of great concern to scientists and physicians are also reports of antibiotic-resistant emerging food pathogens—microorganisms that have not previously been linked to food contamination or were considered epidemiologically insignificant. Since the properties of foodborne pathogens are not always sufficiently recognized, the consequences of the infections are often not easily predictable, and the control of their activity is difficult. The bacteria most commonly identified as emerging foodborne pathogens include Aliarcobacter spp., Aeromonas spp., Cronobacter spp., Vibrio spp., Clostridioides difficile, Escherichia coli, Mycobacterium paratuberculosis, Salmonella enterica, Streptocccus suis, Campylobacter jejuni, Helicobacter pylori, Listeria monocytogenes and Yersinia enterocolitica. The results of our analysis confirm antibiotic resistance and multidrug resistance among the mentioned species. Among the antibiotics whose effectiveness is steadily declining due to expanding resistance among bacteria isolated from food are β-lactams, sulfonamides, tetracyclines and fluoroquinolones. Continuous and thorough monitoring of strains isolated from food is necessary to characterize the existing mechanisms of resistance. In our opinion, this review shows the scale of the problem of microbes related to health, which should not be underestimated. Full article
(This article belongs to the Special Issue Research of Antimicrobial Resistance in the Food Chain)
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